Bettina E. Schirrmeister

Evolution of multicellularity coincided with increased diversification of cyanobacteria and the Great Oxidation Event

Cyanobacteria are among the most diverse prokaryotic phyla, with morphotypes ranging from unicellular to multicellular filamentous forms, including those able to terminally (i.e., irreversibly) differentiate in form and function. It has been suggested that cyanobacteria raised oxygen levels in the atmosphere around 2.45–2.32 billion y ago during the Great Oxidation Event (GOE), hence dramatically changing life on the planet. However, little is known about the temporal evolution of cyanobacterial lineages, and possible interplay between the origin of multicellularity, diversification of cyanobacteria, and the rise of atmospheric oxygen. We estimated divergence times of extant cyanobacterial lineages under Bayesian relaxed clocks for a dataset of 16S rRNA sequences representing the entire known diversity of this phylum. We tested whether the evolution of multicellularity overlaps with the GOE, and whether multicellularity is associated with significant shifts in diversification rates in cyanobacteria. Our results indicate an origin of cyanobacteria before the rise of atmospheric oxygen. The evolution of multicellular forms coincides with the onset of the GOE and an increase in diversification rates. These results suggest that multicellularity could have played a key role in triggering cyanobacterial evolution around the GOE.

Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils

Abstract Cyanobacteria are among the most ancient of evolutionary lineages, oxygenic photosynthesizers that may have originated before 3.0 Ga, as evidenced by free oxygen levels. Throughout the Precambrian, cyanobacteria were one of the most important drivers of biological innovations, strongly impacting early Earths environments. At the end of the Archean Eon, they were responsible for the rapid oxygenation of Earths atmosphere during an episode referred to as the Great Oxidation Event (GOE). However, little is known about the origin and diversity of early cyanobacterial taxa, due to: (1) the scarceness of Precambrian fossil deposits; (2) limited characteristics for the identification of taxa; and (3) the poor preservation of ancient microfossils. Previous studies based on 16S rRNA have suggested that the origin of multicellularity within cyanobacteria might have been associated with the GOE. However, single‐gene analyses have limitations, particularly for deep branches. We reconstructed the evolutionary history of cyanobacteria using genome scale data and re‐evaluated the Precambrian fossil record to get more precise calibrations for a relaxed clock analysis. For the phylogenomic reconstructions, we identified 756 conserved gene sequences in 65 cyanobacterial taxa, of which eight genomes have been sequenced in this study. Character state reconstructions based on maximum likelihood and Bayesian phylogenetic inference confirm previous findings, of an ancient multicellular cyanobacterial lineage ancestral to the majority of modern cyanobacteria. Relaxed clock analyses provide firm support for an origin of cyanobacteria in the Archean and a transition to multicellularity before the GOE. It is likely that multicellularity had a greater impact on cyanobacterial fitness and thus abundance, than previously assumed. Multicellularity, as a major evolutionary innovation, forming a novel unit for selection to act upon, may have served to overcome evolutionary constraints and enabled diversification of the variety of morphotypes seen in cyanobacteria today.

Gene copy number variation and its significance in cyanobacterial phylogeny

BackgroundIn eukaryotes, variation in gene copy numbers is often associated with deleterious effects, but may also have positive effects. For prokaryotes, studies on gene copy number variation are rare. Previous studies have suggested that high numbers of rRNA gene copies can be advantageous in environments with changing resource availability, but further association of gene copies and phenotypic traits are not documented. We used one of the morphologically most diverse prokaryotic phyla to test whether numbers of gene copies are associated with levels of cell differentiation.ResultsWe implemented a search algorithm that identified 44 genes with highly conserved copies across 22 fully sequenced cyanobacterial taxa. For two very basal cyanobacterial species, Gloeobacter violaceus and a thermophilic Synechococcus species, distinct phylogenetic positions previously found were supported by identical protein coding gene copy numbers. Furthermore, we found that increased ribosomal gene copy numbers showed a strong correlation to cyanobacteria capable of terminal cell differentiation. Additionally, we detected extremely low variation of 16S rRNA sequence copies within the cyanobacteria. We compared our results for 16S rRNA to three other eubacterial phyla (Chroroflexi, Spirochaetes and Bacteroidetes). Based on Bayesian phylogenetic inference and the comparisons of genetic distances, we could confirm that cyanobacterial 16S rRNA paralogs and orthologs show significantly stronger conservation than found in other eubacterial phyla.ConclusionsA higher number of ribosomal operons could potentially provide an advantage to terminally differentiated cyanobacteria. Furthermore, we suggest that 16S rRNA gene copies in cyanobacteria are homogenized by both concerted evolution and purifying selection. In addition, the small ribosomal subunit in cyanobacteria appears to evolve at extraordinary slow evolutionary rates, an observation that has been made previously for morphological characteristics of cyanobacteria.

Cyanobacterial evolution during the Precambrian

Life on Earth has existed for at least 3.5 billion years. Yet, relatively little is known of its evolution during the first two billion years, due to the scarceness and generally poor preservation of fossilized biological material. Cyanobacteria, formerly known as blue green algae were among the first crown Eubacteria to evolve and for more than 2.5 billion years they have strongly influenced Earths biosphere. Being the only organism where oxygenic photosynthesis has originated, they have oxygenated Earths atmosphere and hydrosphere, triggered the evolution of plants --being ancestral to chloroplasts-- and enabled the evolution of complex life based on aerobic respiration. Having such a strong impact on early life, one might expect that the evolutionary success of this group may also have triggered further biosphere changes during early Earth history. However, very little is known about the early evolution of this phylum and ongoing debates about cyanobacterial fossils, biomarkers and molecular clock analyses highlight the difficulties in this field of research. Although phylogenomic analyses have provided promising glimpses into the early evolution of cyanobacteria, estimated divergence ages are often very uncertain, because of vague and insufficient tree-calibrations. Results of molecular clock analyses are intrinsically tied to these prior calibration points, hence improving calibrations will enable more precise divergence time estimations. Here we provide a review of previously described Precambrian microfossils, biomarkers and geochemical markers that inform upon the early evolution of cyanobacteria. Future research in micropalaeontology will require novel analyses and imaging techniques to improve taxonomic affiliation of many Precambrian microfossils. Consequently, a better understanding of early cyanobacterial evolution will not only allow for a more specific calibration of cyanobacterial and eubacterial phylogenies, but also provide new dates for the tree of life.

Evolution of cyanobacterial morphotypes

Within prokaryotes cyanobacteria represent one of the oldest and morphologically most diverse phyla on Earth. The rise of oxygen levels in the atmosphere 2.32-2.45 billion years ago is assigned to the photosynthetic activity of ancestors from this phylum. Subsequently cyanobacteria were able to adapt to various habitats evolving a comprehensive set of different morphotypes. In a recent study we showed that this evolution is not a gradual transition from simple unicellular to more complex multicellular forms as often assumed. Instead complexity was lost several times and regained at least once. An understanding of the genetic basis of these transitions would be further strengthened by phylogenomic approaches. However, considering that new methods for phylogenomic analyses are emerging, it is unfortunate that genomes available today are comprised of an unbalanced sampling of taxa. We propose avenues to remedy this by identifying taxa that would improve the representation of phylogenetic diversity in this phylum.

Well-Annotated microRNAomes Do Not Evidence Pervasive miRNA Loss

Abstract microRNAs are conserved noncoding regulatory factors implicated in diverse physiological and developmental processes in multicellular organisms, as causal macroevolutionary agents and for phylogeny inference. However, the conservation and phylogenetic utility of microRNAs has been questioned on evidence of pervasive loss. Here, we show that apparent widespread losses are, largely, an artefact of poorly sampled and annotated microRNAomes. Using a curated data set of animal microRNAomes, we reject the view that miRNA families are never lost, but they are rarely lost (92% are never lost). A small number of families account for a majority of losses (1.7% of families account for >45% losses), and losses are associated with lineages exhibiting phenotypic simplification. Phylogenetic analyses based on the presence/absence of microRNA families among animal lineages, and based on microRNA sequences among Osteichthyes, demonstrate the power of these small data sets in phylogenetic inference. Perceptions of widespread evolutionary loss of microRNA families are due to the uncritical use of public archives corrupted by spurious microRNA annotations, and failure to discriminate false absences that occur because of incomplete microRNAome annotation.

Geitlerinema sp. PCC 8501

Protein sequences of Geitlerinema sp. PCC 8501. Annotated with Prokka (http://www.vicbioinformatics.com/software.prokka.shtml).